The establishment of a molecular diagnostic platform for mitochondrial diseases: From conventional to next-generation sequencing

Background: The aim of this study was to create a molecular diagnostic platform and establish a diagnostic pipeline for patients highly suspected of mitochondrial disorders. The effectiveness of three methods, namely, traditional restriction fragment length polymorphism-polymerase chain reaction (RF...

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Main Authors: Ni-Chin Tsai, Chai-Wai Liou, Yin-Hua Cheng, Hao-Ting Lien, Tzu-Ling Lin, Tsu-Kung Lin, Min-Yu Lan, Pi-Lien Hung, Tzu-Jou Wang, Chen-Hao Lee, Yi-Chih Liang, Kuo-Chung Lan
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Language:English
Published: Elsevier 2025-04-01
Series:Biomedical Journal
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Online Access:http://www.sciencedirect.com/science/article/pii/S2319417024000738
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author Ni-Chin Tsai
Chai-Wai Liou
Yin-Hua Cheng
Hao-Ting Lien
Tzu-Ling Lin
Tsu-Kung Lin
Min-Yu Lan
Pi-Lien Hung
Tzu-Jou Wang
Chen-Hao Lee
Yi-Chih Liang
Kuo-Chung Lan
author_facet Ni-Chin Tsai
Chai-Wai Liou
Yin-Hua Cheng
Hao-Ting Lien
Tzu-Ling Lin
Tsu-Kung Lin
Min-Yu Lan
Pi-Lien Hung
Tzu-Jou Wang
Chen-Hao Lee
Yi-Chih Liang
Kuo-Chung Lan
author_sort Ni-Chin Tsai
collection DOAJ
description Background: The aim of this study was to create a molecular diagnostic platform and establish a diagnostic pipeline for patients highly suspected of mitochondrial disorders. The effectiveness of three methods, namely, traditional restriction fragment length polymorphism-polymerase chain reaction (RFLP-PCR), Sanger sequencing for hotspot detection and whole mitochondrial DNA (mtDNA), and third-generation (Nanopore) whole mtDNA sequencing, will be compared in diagnosing patients with suspected primary mitochondrial diseases (PMDs). The strengths and limitations of different methods are also discussed. Material and methods: A single-center prospective cohort study was conducted to validate the diagnostic pipeline for suspected mitochondrial diseases. In the first stage, a PCR-based method with five sets of primers was used to screen for eight hotspots (m.3243A > G, m.3460G > A, m.8344A > G, m.8993T > G, m.9185T > C, m.11778G > A, m.13513G > A, and m.4977deletion) using either RFLP or direct Sanger sequencing. Sanger sequencing was also used to confirm the RFLP-positive samples. In the second stage, for samples with negative screening results for the eight hotspots, mitochondrial whole-genome sequencing was performed using Sanger sequencing or third-generation nanopore sequencing. Results: Between June 2020 and May 2023, 30 patients from ages 0 to 63 with clinically suspected mitochondrial disease were enrolled. The positive yield for the diagnosis of PMDs was 8/30 = 26.7%, and the sensitivity of the heteroplasmy level for the RFLP-based method was approximately 5%. The remaining 22 patients who tested negative at the first stage were tested using Sanger sequencing or the third-generation sequencing Nanopore, and all tested negative for pathological mtDNA mutations. Compared to the Sanger sequencing method, the results of RFLP-PCR were compromised by the limitations of incomplete RFLP enzyme digestion. For whole-genome sequencing of mtDNA, Sanger sequencing, instead of nanopore sequencing, is preferred at our institution because of its cost-effectiveness. Conclusions: In our highly selective cohort, most tested positive in the first stage of the 8 hot spots screen. Sanger sequencing is a conventional and accurate method for mitochondrial disease screening, at least for the most common hot spots in the region. The results revealed that Sanger sequencing is an accurate method with the benefit of being more cost-effective. This integral platform of molecular diagnosis bears the advantages of being relatively low cost and having a shorter reporting time, facilitating crucial identification of patients with clinical evidence of such disorders. This diagnostic flowchart has also been translated into routine clinical use in the tertiary hospital.
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spelling doaj-art-6de7db93513d45dfbee8ccdfe9efd0372025-08-20T02:05:36ZengElsevierBiomedical Journal2319-41702025-04-0148210077010.1016/j.bj.2024.100770The establishment of a molecular diagnostic platform for mitochondrial diseases: From conventional to next-generation sequencingNi-Chin Tsai0Chai-Wai Liou1Yin-Hua Cheng2Hao-Ting Lien3Tzu-Ling Lin4Tsu-Kung Lin5Min-Yu Lan6Pi-Lien Hung7Tzu-Jou Wang8Chen-Hao Lee9Yi-Chih Liang10Kuo-Chung Lan11Graduate Institute of Clinical Medicine, College of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan; Center for Mitochondrial Research and Medicine, Kaohsiung Chang Gung Memorial Hospital, Kaohsiung, Taiwan; Department of Obstetrics and Gynecology, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, Taiwan; Center for Menopause and Reproductive Medicine Research, Kaohsiung Chang Gung Memorial Hospital, Kaohsiung, TaiwanCenter for Mitochondrial Research and Medicine, Kaohsiung Chang Gung Memorial Hospital, Kaohsiung, Taiwan; Department of Neurology, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, TaiwanCenter for Mitochondrial Research and Medicine, Kaohsiung Chang Gung Memorial Hospital, Kaohsiung, Taiwan; Department of Obstetrics and Gynecology, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, Taiwan; Center for Menopause and Reproductive Medicine Research, Kaohsiung Chang Gung Memorial Hospital, Kaohsiung, TaiwanCenter for Mitochondrial Research and Medicine, Kaohsiung Chang Gung Memorial Hospital, Kaohsiung, Taiwan; Department of Obstetrics and Gynecology, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, TaiwanCenter for Mitochondrial Research and Medicine, Kaohsiung Chang Gung Memorial Hospital, Kaohsiung, Taiwan; Center for Menopause and Reproductive Medicine Research, Kaohsiung Chang Gung Memorial Hospital, Kaohsiung, TaiwanCenter for Mitochondrial Research and Medicine, Kaohsiung Chang Gung Memorial Hospital, Kaohsiung, Taiwan; Department of Neurology, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, TaiwanCenter for Mitochondrial Research and Medicine, Kaohsiung Chang Gung Memorial Hospital, Kaohsiung, Taiwan; Department of Neurology, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, TaiwanCenter for Mitochondrial Research and Medicine, Kaohsiung Chang Gung Memorial Hospital, Kaohsiung, Taiwan; Department of Pediatrics, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, TaiwanCenter for Mitochondrial Research and Medicine, Kaohsiung Chang Gung Memorial Hospital, Kaohsiung, Taiwan; Department of Pediatrics, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, TaiwanDepartment of Pediatrics, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, TaiwanDepartment of Pediatrics, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, TaiwanGraduate Institute of Clinical Medicine, College of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan; Center for Mitochondrial Research and Medicine, Kaohsiung Chang Gung Memorial Hospital, Kaohsiung, Taiwan; Department of Obstetrics and Gynecology, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, Taiwan; Center for Menopause and Reproductive Medicine Research, Kaohsiung Chang Gung Memorial Hospital, Kaohsiung, Taiwan; Department of Obstetrics and Gynecology, Jen-Ai Hospital, Taichung, Taiwan; Corresponding author. Department of Obstetrics and Gynecology, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, Taiwan.Background: The aim of this study was to create a molecular diagnostic platform and establish a diagnostic pipeline for patients highly suspected of mitochondrial disorders. The effectiveness of three methods, namely, traditional restriction fragment length polymorphism-polymerase chain reaction (RFLP-PCR), Sanger sequencing for hotspot detection and whole mitochondrial DNA (mtDNA), and third-generation (Nanopore) whole mtDNA sequencing, will be compared in diagnosing patients with suspected primary mitochondrial diseases (PMDs). The strengths and limitations of different methods are also discussed. Material and methods: A single-center prospective cohort study was conducted to validate the diagnostic pipeline for suspected mitochondrial diseases. In the first stage, a PCR-based method with five sets of primers was used to screen for eight hotspots (m.3243A > G, m.3460G > A, m.8344A > G, m.8993T > G, m.9185T > C, m.11778G > A, m.13513G > A, and m.4977deletion) using either RFLP or direct Sanger sequencing. Sanger sequencing was also used to confirm the RFLP-positive samples. In the second stage, for samples with negative screening results for the eight hotspots, mitochondrial whole-genome sequencing was performed using Sanger sequencing or third-generation nanopore sequencing. Results: Between June 2020 and May 2023, 30 patients from ages 0 to 63 with clinically suspected mitochondrial disease were enrolled. The positive yield for the diagnosis of PMDs was 8/30 = 26.7%, and the sensitivity of the heteroplasmy level for the RFLP-based method was approximately 5%. The remaining 22 patients who tested negative at the first stage were tested using Sanger sequencing or the third-generation sequencing Nanopore, and all tested negative for pathological mtDNA mutations. Compared to the Sanger sequencing method, the results of RFLP-PCR were compromised by the limitations of incomplete RFLP enzyme digestion. For whole-genome sequencing of mtDNA, Sanger sequencing, instead of nanopore sequencing, is preferred at our institution because of its cost-effectiveness. Conclusions: In our highly selective cohort, most tested positive in the first stage of the 8 hot spots screen. Sanger sequencing is a conventional and accurate method for mitochondrial disease screening, at least for the most common hot spots in the region. The results revealed that Sanger sequencing is an accurate method with the benefit of being more cost-effective. This integral platform of molecular diagnosis bears the advantages of being relatively low cost and having a shorter reporting time, facilitating crucial identification of patients with clinical evidence of such disorders. This diagnostic flowchart has also been translated into routine clinical use in the tertiary hospital.http://www.sciencedirect.com/science/article/pii/S2319417024000738Mitochondrial DNA amplificationMitochondrial diseaseMolecular diagnostic platformWhole mitochondrial DNA sequencing
spellingShingle Ni-Chin Tsai
Chai-Wai Liou
Yin-Hua Cheng
Hao-Ting Lien
Tzu-Ling Lin
Tsu-Kung Lin
Min-Yu Lan
Pi-Lien Hung
Tzu-Jou Wang
Chen-Hao Lee
Yi-Chih Liang
Kuo-Chung Lan
The establishment of a molecular diagnostic platform for mitochondrial diseases: From conventional to next-generation sequencing
Biomedical Journal
Mitochondrial DNA amplification
Mitochondrial disease
Molecular diagnostic platform
Whole mitochondrial DNA sequencing
title The establishment of a molecular diagnostic platform for mitochondrial diseases: From conventional to next-generation sequencing
title_full The establishment of a molecular diagnostic platform for mitochondrial diseases: From conventional to next-generation sequencing
title_fullStr The establishment of a molecular diagnostic platform for mitochondrial diseases: From conventional to next-generation sequencing
title_full_unstemmed The establishment of a molecular diagnostic platform for mitochondrial diseases: From conventional to next-generation sequencing
title_short The establishment of a molecular diagnostic platform for mitochondrial diseases: From conventional to next-generation sequencing
title_sort establishment of a molecular diagnostic platform for mitochondrial diseases from conventional to next generation sequencing
topic Mitochondrial DNA amplification
Mitochondrial disease
Molecular diagnostic platform
Whole mitochondrial DNA sequencing
url http://www.sciencedirect.com/science/article/pii/S2319417024000738
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